The Food and Agricultural Organization has provided an estimate of the alarmingly increasing human population, expected to reach 8–9 billion by 2030 (FAO, 2010). As a result of increasing urbanization and industrialization, threats to the environment have increased, leading to the shrinkage of agricultural land on one hand and causing significant declines in crop growth on the other hand. Abiotic stresses have the potential to restrict the growth of crop plants considerably, therefore leading to significant yield losses and posing a potential threat to global food security (Mahalingam, 2015).

Environmental stresses are detrimental to the growth of plants. Drought, salinity, heavy metal contamination, flooding, temperature (cold and high), and ultraviolet radiation are the key abiotic factors that modulate the growth of plants to the extent that a reduction in yield is a certain effect. Changes in the climate patterns of different regions have resulted in shifts in vegetation, and approximately 2,000 million hectares of land worldwide has been affected by increased water scarcity and salinization (El-Beltagy and Madkour, 2012). It is believed that approximately 25% of global agricultural land is affected by drought and approximately 5–7% is affected by salt (Ruiz-Lozano et al., 2012). Abiotic stresses inhibit plant growth by reducing water uptake and altering plant physiological and biochemical processes (Ahmad et al., 2010; Hashem et al., 2016). Heavy metals, including cadmium, lead, and mercury, are toxic and are mostly present in soils at low concentrations. However, due to their high mobility in the soil–plant system, they are readily taken up by plants and delivered to the shoot (Hart et al., 1998). Increases in metal concentrations cause retardation of growth, leading to necrosis, altered nutrient uptake, reduced enzyme activity and hence phytotoxicity (Groppa et al., 2012).

A better understanding of the different tolerance strategies for maintaining crop productivity through the manipulation of environmental conditions can be helpful for maintaining the maximum genetic potential of crops as much as possible. Phytohormones are important growth regulators synthesized in defined organs of the plant that have a prominent impact on plant metabolism (Kazan, 2013) and play an important role in the mitigation of abiotic stresses (Teale et al., 2006; Hu et al., 2013). However, abiotic stresses alter the endogenous levels of phytohormones, such as auxins, gibberellins, abscisic acid (ABA), jasmonic acid and salicylic acid (SA), which causes plant growth perturbations (Debez et al., 2001; Egamberdieva, 2009; Khan et al., 2014). Drought and salt stress have also been reported to inhibit phytohormone concentrations in plant tissue.

There has been enormous progress in research regarding crop improvement in hostile environments, and the role of some tools, such as microbial technology and genetic engineering, has been acknowledged. Accordingly, several strategies for improving plant stress tolerance by root-associated microbes, such as a low-input biotechnology, have been proposed (Khan et al., 2013). Plant-associated microbes live in plant tissue endophytically or symbiotically or they colonize the root surface and cooperate with each other by producing various metabolically active substances (Egamberdieva, 2011, 2012; Berg et al., 2013; Asaf et al., 2017). The stimulation of plant growth and nutrient acquisition by beneficial rhizobacteria has been correlated to the biosynthesis of plant growth regulators, including auxins (Etesami et al., 2015; Pereira et al., 2016), gibberellins (Khan et al., 2014), cytokinins (Kudoyarova et al., 2014), and ABA (Sgroy et al., 2009). The microbial regulators modulate plant hormone levels in plant tissue, and they have been found to have effects that are similar to exogenous phytohormone application (Egamberdieva, 2009; Turan et al., 2014; Shahzad et al., 2016). Based on the currently available studies on the effect of phytohormones on plant stress tolerance, this review attempts to improve the understanding of microbial phytohormones and their interactions with plants by assessing their influence on plant physiological and morphological properties. Based on important studies on the negative effect of abiotic stresses on plant growth regulators, we have also presented some potential traits of microbial phytohormones that can be used to increase plant growth and tolerance to stress factors. In this review, we will focus on the plant growth regulators synthesized by root-associated microbes, their diversity, physiology and their involvement in stress tolerance of plants to abiotic stresses including drought, salt, and heavy metals.

Soils are sources of diverse organisms, including fungi, bacteria, and plants (Mendes et al., 2013). Plant roots are heavily colonized with microorganisms (compared to soil and other habitats) because of the rich nutrient component of root exudates (Schlaeppi and Bulgarelli, 2015; Hashem et al., 2016). The rhizosphere is a relatively nutrient-rich environment containing amino acids, sugars, fatty acids and other organic compounds, which attract microbes (Vorholt, 2012) that utilize the various nutrients released by the root. In turn, the microbes synthesize biologically active compounds, including phytohormones (auxins, cytokinins, gibberellins, and ABA), antifungal compounds, enzymes, and compatible solutes. These microbial metabolites play a vital role in plant growth, nutrition and development (Ruiz-Lozano et al., 2012; Sorty et al., 2016; Egamberdieva et al., 2017a). They can stimulate plant growth development, provide resistance to various abiotic and biotic stress factors, improve nutrient acquisition and protect plants from various soil-borne pathogens (Grover et al., 2013; Cho et al., 2015). The beneficial interactions of microbes in plants, their positive effect on plant growth and their improvement of stress tolerance under extreme environmental conditions have been extensively reviewed by Nadeem et al. (2014), and the mechanisms utilized by plant growth-promoting bacteria have been reviewed by Forni et al. (2017). There are several mechanisms of plant growth stimulation, plant protection and alleviation of salt stress by PGPR, such as nitrogen fixation; synthesis of osmoprotectants, exopolysaccharides, 1-aminocyclopropane-1-carboxylate (ACC) deaminase, cell wall degrading enzymes, and phytohormones; modulation of antioxidant enzymes or nutrients; and solubilization of minerals, such as phosphorus, and potassium (Berg et al., 2013; Wang Q. et al., 2016; Mishra et al., 2017). The microbes mitigate stress responses by regulating the nutritional and hormonal balance in plants and inducing systemic tolerance to stress. One of the mechanisms of improvement of plant growth and stress tolerance by microbes is their phytohormone synthesizing ability in the rhizosphere or root tissue (Etesami et al., 2015). Microbial phytohormones affect the metabolism of endogenous growth regulators in plant tissue (Hashem et al., 2016; Sorty et al., 2016) and play a key role in changing root morphology upon exposure to drought, salinity, extreme temperature and heavy metal toxicity (Spaepen et al., 2008; Khan et al., 2011).

Root-associated microbes, including free living, symbiotic or endophytic microbes, can produce various type of phytohormones and belong to different genera and species (Sgroy et al., 2009). For example, Sorty et al. (2016) isolated diverse groups of organisms belonging to Acinetobacter, Bacillus, Enterobacter, Pantoea, Pseudomonas, Rhizobium, and Sinorhizobium from halotolerant weed (Psoralea corylifolia L.), and Egamberdieva et al. (2016) found Arthrobacter, Bacillus, Enterobacter, Pseudomonas, Rhizobium, Brevibacillus, Cellulosimicrobium, Mycobacterium, Ochrobactrum, Paenibacillus, and Pseudoxanthomonas associated with soybean root. The IAA-producing Mycobacterium species was observed in the rhizosphere of orchid (Tsavkelova et al., 2007), and Azotobacter, Azospirillum, Cellulomonas, Mycoplana, and Rahnella were found in the wheat rhizosphere (Egamberdiyeva and Hoflich, 2003; Egamberdieva et al., 2008). In other reports, Pseudomonas spp. (Lawongsa et al., 2008), Arthrobacter spp. (Piccoli et al., 2011), and Enterobacter, Pseudomonas, and Stenotrophomonas species were associated with plants that produced IAA (Khan and Doty, 2009). Piccoli et al. (2011) isolated the endophytic diazotrophic bacterium Arthrobacter koreensis which produce ABA, IAA, GA3 and jasmonic acid from the roots of the halophyte shrub Prosopis strombulifera. The endophytic strains of Klebsiella and Enterobacter isolates from sugar cane synthesize IAA (de Santi Ferrara et al., 2012). Mishra et al. (2017) isolated bacteria with IAA production ability from extreme environments, which were identified as Pseudomonas spp. and Ochrobactrum spp. In other studies Halomonas desiderata, Bacillus megaterium, Bacillus cereus, Bacillus subtilis, Escherichia coli, and Pseudomonas fluorescens G20-18 were reported to synthesize cytokinins (Salamone et al., 2001; Karadeniz et al., 2006; Großkinsky et al., 2016). Bacterial isolates from the rhizosphere of a vegetable (bitter gourd) belonging to genera Bacillus, Klebsiella, Leifsonia, and Enterobacter were able to produce IAA and improved maize growth in Cd-contaminated soil (Ahmad et al., 2016).

Naz et al. (2009) also observed cytokinin-producing species, such as Arthrobacter, Bacillus, Azospirillum, and Pseudomonas, that stimulated the root development of plants. ABA was also detected in root-associated microbes from various plants. Karadeniz et al. (2006) reported Proteus mirabilis, Phaseolus vulgaris, Klebsiella pneumoniae, B. megaterium, and B. cereus as ABA-producing bacteria. Species such as Bacillus pumilus, Bacillus licheniformis, Acetobacter sp., Bacillus sp., Azospirillium sp. were found among gibberellin-producing strains (Gutiérrez-Mañero et al., 2001; Bottini et al., 2004). Salomon et al. (2014) observed ABA-producing B. licheniformis Rt4M10 and P. fluorescens Rt6M10 in the rhizosphere of Vitis vinifera. Achromobacter xylosoxidans SF2, isolated from sunflower roots, was also able to produce ABA in minimal medium (Forchetti et al., 2007). Among IAA-producing bacteria associated with plants grown under saline soil, Rhizobia have also been shown to synthesize auxins, cytokinins and abscicic acids, increase plant growth and development and improve the yield of agricultural crops (Hayat et al., 2008). Actinobacteria have also been found to produce IAA, CK, GB-like substances (Shutsrirung et al., 2013; Vijayabharathi et al., 2016). Ruanpanun et al. (2010) found high IAA-producing nematophagous actinomycete and fungal isolates, such as Aspergillus and Streptomyces. In other studies, Streptomyces sp. Isolated from medicinal plant species Taxus chinensis and Artemisia annua showed IAA synthesis ability (Lin and Xu, 2013). Shutsrirung et al., 2013 reported IAA production in endophytic actinomycetes Streptomyces, Nocardia, Nocardiopsis, Spirillospora, Microbispora, and Micromonospora associated with mandarin.

The stress tolerance ability of bacterial strains provides important benefits to plants. The ability of root-associated microbes to synthesize phytohormones is typically not hampered by high salt concentrations (Egamberdieva and Kucharova, 2009). For example, phytohormone synthesis by endophytic actinobacteria Streptomyces coelicolor DE07 and Streptomyces geysiriensis DE27 was not inhibited under water stress (Yandigeri et al., 2012). The production of IAA by A. brasilense in osmotic stress conditions was higher than that of osmosensitive A. brasilense Sp7 (Nabti et al., 2007). In another study, Pseudomonas putida, Pseudomonas extremorientalis, Pseudomonas chlororaphis, and P. aurantiaca were able to produce IAA in a 4% NaCl conditions (Egamberdieva and Kucharova, 2009). Pseudomonas sp. and Bacillus sp. strains were able to produce IAA under high salt conditions (200–400 mM NaCl) and increased the plant biomass of Sulla carnosa under salt stress (Hidri et al., 2016).

The biosynthesis of phytohormones differs by bacterial strain. For example, Bacillus and Pseudomonas strains synthesized IAA concentrations up to 2.2 μg mL^-1, GA3 production by A. xylosoxidans and B. halotolerans was between 36.5 and 75.5 μg mL^-1 (Sgroy et al., 2009). In addition, ABA production was 0.3, 1.8, and 4.2 μg mL^-1 in the culture medium of L. fusiformis (Ps14), B. subtilis (Ps8), and P. putida (Ps30), respectively. In another study, Bacillus amyloliquefaciens associated with rice (Oryza sativa L.) synthesized gibberellins, and the quantities of GA differed, e.g., 17.8 ng mL^-1 for GA20, 5.7 ng mL^-1 for GA36, 5.6 ng mL^-1 for GA24, 1.02 ng mL^-1 for GA4, 0.7 ng mL^-1 for GA53, 0.08 ng mL^-1 for GA5, and 0.01 ng mL^-1 for GA8 (Shahzad et al., 2016). Endophytic fungi Aspergillus fumigatus associated with soybean roots synthesized gibberellins, such as GA4 (24.8 ng mL^-1), GA9 (1.2 ng mL^-1), and GA12 (9.8 ng mL^-1) (Khan et al., 2011). Several studies reported SA production by root-associated bacteria, e.g., B. licheniformis MML2501 (18 μg mL^-1) (Shanmugam and Narayanasamy, 2008), and Pseudomonas sp. PRGB06 (6.8 μg mL^-1) (Indiragandhi et al., 2008).

Microbes synthesize low amounts of phytohormones and improve stress tolerance and plant growth under various stress conditions, including salinity, heat, drought and metal toxicity, as reported in many studies (Sgroy et al., 2009; Egamberdieva et al., 2011, 2017b; Liu Y. et al., 2013). The beneficial effect of phytohormone-producing microbes on alleviating abiotic stress in plants was reported in numerous studies (Figure 1; Khan and Doty, 2009; Ngumbi and Kloepper, 2014; Hashem et al., 2016). Some examples of phytohormone-producing bacteria and their ability to mitigate abiotic stress are given in Table 1. Many studies have reported the positive effects of bacteria associated with plants and IAA production on plant growth stimulation under abiotic stress conditions. For example, bacterial strains Curtobacterium flaccumfaciens E108 and Ensifer garamanticus E110 isolated from Hordeum secalinum stimulated plant biomass and salt stress resistance in barley (Cardinale et al., 2015). The root-colonizing halotolerant bacterium B. licheniformis HSW-16 was able to mitigate salt stress-induced damage and stimulate the growth of wheat through the production of IAA under saline soil conditions (Singh and Jha, 2016). Similar observations were reported by Upadhyay et al. (2012) in which salt-tolerant bacterial strains B. subtilis and Arthrobacter sp. increased wheat biomass and total soluble sugars and reduced sodium concentration in plant tissue. Sorty et al. (2016) isolated salt-tolerant strain Enterobacter sp. NIASMVII from halotolerant weed (Psoralea corylifolia L.), which produces IAA (0.22 and 25.58 μg mL^-1) and enhances seed germination of wheat (Triticum aestivum L.). In another study, Pseudomonas spp. isolated from extreme environments (close to the sites of volcanos) synthesized IAA under salt stress (500 mM NaCl) and high temperature (40°C), and they were able to stimulate increases in the root and shoot biomass of maize (Mishra et al., 2017). According to Bianco and Defez (2009), protection of plants from negative effects of abiotic stress by IAA is related to enhanced cellular defense systems. Several salt-tolerant strains synthesizing IAA in culture medium, namely, Serratia plymuthica RR-2-5-10, Stenotrophomonas rhizophila e-p10, P. fluorescens SPB2145, P. extremorientalis TSAU20, and P. fluorescens PCL1751, improved cucumber biomass and yield in greenhouse conditions (9–24%) (Egamberdieva et al., 2011). Root-associated IAA-producing bacteria were found to improve drought stress in plants. Marulanda et al. (2009) observed increased plant biomass in clover (Trifolium repens L.) after seed treatment with P. putida and B. megaterium under drought, and they found a correlation between these changes and increased IAA. IAA-producing bacteria were also found to improve plant growth and development under nutrient-poor soil conditions. Serratia sp. isolated from chickpea nodules was found to produce IAA, which led to an increased grain yield of chickpea in nutrient-deficient soil (Zaheer et al., 2016). Many fungal species were also able to produce plant growth regulators and alter plant root system and physiology. Contreras-Cornejo et al. (2009) observed increased lateral root formation, root hair growth and modified root system architecture from Trichoderma virens inoculation, which resulted in increased plant biomass of Arabidopsis thaliana.

Microbial phytohormones also play an important role in metal-plant interactions, improving phytoextraction by plants. A. xylosoxidans Ax10 improved the root system of the Brassica juncea plant through IAA production activities, which increased copper phytoextraction (Ma et al., 2008). Similar results were observed by Zaidi et al. (2006) in which B. subtilis synthesizing IAA stimulated root growth and Ni accumulation in the Indian mustard plant (B. juncea L.). B. megaterium MCR-8, which produced auxin at a concentration of 68.5 mg 25 mL^-1, alleviated Ni stress in Vinca rosea and stimulated root and shoot growth. In addition, plant treatment with B. megaterium MCR-8 increased the accumulation of total phenols, flavonoids and defense-related enzymes, such superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), and ascorbate peroxidase (APX), compared to uninoculated plants under Ni stress (Khan et al., 2017). In another study, Ahmad et al. (2016) observed inhibited seed germination and seedling growth of maize by Cd stress, whereas Cd-tolerant and IAA-producing bacteria Leifsonia sp. and Bacillus sp. significantly increased shoot and root growth of maize in Cd-contaminated soil compared to controls. Similar observations were reported by Dourado et al. (2013) in which Cd-tolerant multi-tolerant bacteria Burkholderia sp. SCMS54 produced IAA and improved plant growth and stress tolerance of tomato to Cd stress. Islam et al. (2016) reported that Cr toxicity significantly inhibited maize growth, negatively affecting its physiological processes, such as photosynthetic pigment and carbohydrate metabolism, and increasing its levels of proline, H₂O₂, and MDA. In these conditions, Cr-resistant P. mirabilis isolates T2Cr and CrP450, combined with SA, mitigated the toxic effect of Cr, improved the root and shoot growth of maize and reduced oxidative stress in maize tissue by elevating its antioxidant activities.

The tripartite interaction of root-associated microbes with symbiotic microbes and the host plant is also a mutualistic interaction that improves plant growth under stress through the induction of osmoregulation, hormonal balance, biochemical processes and changes in metabolic interfaces among partners (Nadeem et al., 2014; Park et al., 2017). IAA-producing B. subtilis NUU4 in combination with Mesorhizobium ciceri IC53 stimulated root and shoot biomass and improved nodule formation in chickpea (Cicer arietinum L.) under salt stress, as compared to uninoculated plants and plants inoculated with Mesorhizobium ciceri IC53 alone (Egamberdieva et al., 2017c) (Figure 2).

The positive effect on root development by cytokinin-producing bacterial strains was also reported in many studies. For example, inoculation of maize with cytokinin-producing bacteria Micrococcus luteus chp37 isolated from the desert of Pakistan stimulated shoot and root biomass by 54% and modulated the physiological properties of the plant, including photosynthetic pigments, under drought conditions (Raza and Faisal, 2013). The cytokinin-producing root-associated bacteria strains Arthrobacter, Bacillus, Azospirillum, and Pseudomonas increased soybean shoot and root biomass as well as proline content in plant tissue under salt stress (Naz et al., 2009). A similar observation was reported by Liu F. et al. (2013) in which cytokinin-producing B. subtilis stimulated root biomass of Platycladus orientalis (oriental thuja) by 13.9% and increased cytokinin concentration of 47.52% in leaves relative to respective controls under water stress conditions. The higher content of cytokinin in plant tissue contributed to stomatal opening and alleviated some of the detrimental effects of water stress.

Aspergillus fumigatus produced gibberellins, such as GA4 (24.8 ng mL^-1), GA9 (1.2 ng mL^-1), and GA12 (9.8 ng mL^-1), which increased photosynthetic pigments, and shoot biomass of soybean under salt stress (Khan et al., 2011). Azospirillum lipoferum, which synthesizes GA, increased the stress tolerance of wheat to drought (Creus et al., 2004). Waqas et al. (2012) also reported improved salt and drought stress tolerance in cucumber plant by GA-producing endophytic fungi Phoma glomerata LWL2 LWL3, which produced GA1 (8.720 ng mL^-1), GA3 (2.420 ng mL^-1) and GA4 (0.220 ng mL^-1), and Penicillium sp., which produced GA1 (5.33 ng mL^-1) and GA3 (3.42 ng mL^-1) in culture filtrate. The fungal inoculation resulted in increased root and shoot growth and nutrient uptake, and reduced stress by down-regulating ABA and modifying SA and jasmonic acid concentrations in plant tissue. It is known that ABA and SA act as defense signaling constituents (Shinozaki and Yamaguchi-Shinozaki, 2007).

Salomon et al. (2014) observed ABA production by B. licheniformis and P. fluorescens that stimulated plant growth of grapevine under water stress by inducing ABA synthesis. Shahzad et al. (2017) reported ABA production by Bacillus amyloliquefaciens RWL-1 (0.32 ± 0.015–0.14 ± 0.030 ng mL^-1) under normal and saline conditions. Bacterial inoculation significantly increased root and shoot growth and the concentration of SA in plant tissue of rice under salt stress conditions. Park et al. (2017) isolated Bacillus aryabhattai strain SRB02 from the rhizosphere of soybean, and it significantly promoted the plant biomass and nodule number of soybean. The strains produced up to 2 ng mL^-1 ABA in culture and increased the drought stress tolerance of soybean through stomatal closure under high temperatures (38°C) relative to control plants.

Similar to the effects of other phytohormones, SA-producing endophytic bacteria A. xylosoxidans and B. pumilus also enhanced the biomass of sunflower seedlings under drought conditions (Forchetti et al., 2010). Similar observations were reported by Lavania and Nautiyal (2013) in which salt-tolerant SA-producing Serratia marcescens NBRI1213 stimulated root and shoot growth as well as nutrient acquisition by maize, and furthermore increased plant stress tolerance to salinity.

Some bacteria may produce several types of phytohormones in plant tissue that interact to modulate important physiological processes in plants, including hormonal balance. Sphingomonas sp. LK11 and Serratia marcescens TP1 produced 12.31 and 10.5 μM mL^-1 of IAA in the culture broths, which stimulated root and shoot growth of soybean through increases in ABA and gibberellin and a decrease in jasmonic acid content compared to levels in the control plants (Asaf et al., 2017). Trichoderma asperellum Q1, which produces IAA, GA and ABA, stimulated the biomass fresh weight of cucumber seedlings under salt stress in comparison to untreated control plants (Zhao and Zhang, 2015). In addition, the concentration of phytohormones IAA, GA and ABA in cucumber leaves were also increased after application of Trichoderma asperellum Q1 under salt stress. Similar observations were reported by Park et al. (2017) for soybean inoculated with Bacillus aryabhattai SRB02, which produces IAA, GA, and ABA. The root and shoot growth and heat stress of soybean plants increased after bacterial inoculation. In addition, higher concentrations of IAA, JA, GA12, GA4, and GA7 were observed in plant tissue of Bacillus aryabhattai SRB02-treated plants. Similar observations were reported for maize inoculated with ABA-producing Azospirillum lipoferum and A. brasilense sp. 245 in which bacterial treatment resulted in an increased concentration of ABA in plant tissue (Cohen et al., 2015). These studies demonstrate the involvement of phytohormone modulation in plant tissue by plant-associated microbes that induce the stress tolerance of plants.

Overall, evidence was provided that the exogenous application of phytohormones of microbial origin is an important tool for increasing the abiotic and biotic stress tolerance of plants, providing potential practical applications under changing or extreme environmental conditions. The beneficial effects on plants mediated by microbes, such as the stimulation of plant growth, tolerance to abiotic stresses and resistance to pathogens, are based on the microbes’ ability to produce auxins, gibberellins, SA, ABA, and cytokinins in plant tissues. Thus, plant-associated microbes hold the potential to modulate hormone levels and metabolism in plant tissue, especially in biochemical processes that can prevent the damaging effects of external stresses, such as drought, salinity, nutrient deficiency, or heavy metal contamination. Optimizing phytohormone balance in plant tissues under stress by beneficial microbes could be a crucial challenge in the development of sustainable approaches to crop production. More experimental studies on various plant species are needed to determine whether these are plant-specific traits and to better understand the mechanisms involved in the interactions between microbial metabolites and the host that help plants optimize their responses in hostile environments. More specifically, it can be worthwhile to employ loss-of-function or gain-of-function genetic mechanisms to explore the associated mechanisms or reveal the antagonistic or synergistic interactions of phytohormones. The identification of receptors leading to the expression of specific genes after the application of a microbial phytohormone is also an important topic. Furthermore, studies on the performance of phytohormone-producing microbes in field experiments are necessary, and they should include competition for nutrients and niches between the microbial inoculant and the indigenous microflora. Moreover, investigations of host-microbe-stress interactions and their involved mechanisms using omics-based approaches, such as proteomics, genomics, metagenomics, and metabolomics, are needed.

DE, SW, and EA designed and wrote the manuscript. AH and AA edited and helped in finalizing the manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.